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Title: H2-Independent Growth of the Hydrogenotrophic Methanogen Methanococcus maripaludis

Abstract

Hydrogenotrophic methanogenic Archaea require reduced ferredoxin as an anaplerotic source of electrons for methanogenesis. H2 oxidation by the hydrogenase Eha provides these electrons, consistent with an H2 requirement for growth. Here we report the identification of alternative pathways of ferredoxin reduction in Methanococcus maripaludis that operate independently of Eha to stimulate methanogenesis. A suppressor mutation that increased expression of the glycolytic enzyme glyceraldehyde-3-phosphate:ferredoxin oxidoreductase resulted in a strain capable of H2-independent ferredoxin reduction and growth with formate as the sole electron donor. In this background, it was possible to eliminate all seven hydrogenases of M. maripaludis. Alternatively, carbon monoxide oxidation by carbon monoxide dehydrogenase could also generate reduced ferredoxin that feeds into methanogenesis. In either case, the reduced ferredoxin generated was inefficient at stimulating methanogenesis, resulting in a slow growth phenotype. As methanogenesis is limited by the availability of reduced ferredoxin under these conditions, other electron donors, such as reduced coenzyme F420, should be abundant. Indeed, when F420-reducing hydrogenase was reintroduced into the hydrogenase-free mutant, the equilibrium of H2 production via an F420-dependent formate:H2 lyase activity shifted markedly toward H2 compared to the wild type.

Authors:
 [1];  [1];  [1];  [1]
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  1. Univ. of Washington, Seattle, WA (United States). Dept. of Microbiology
Publication Date:
Research Org.:
Univ. of Washington, Seattle, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1626081
Grant/Contract Number:  
FG02-05ER15709
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 4; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology

Citation Formats

Costa, Kyle C., Lie, Thomas J., Jacobs, Michael A., and Leigh, John A. H2-Independent Growth of the Hydrogenotrophic Methanogen Methanococcus maripaludis. United States: N. p., 2013. Web. doi:10.1128/mbio.00062-13.
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Costa, Kyle C., Lie, Thomas J., Jacobs, Michael A., & Leigh, John A. H2-Independent Growth of the Hydrogenotrophic Methanogen Methanococcus maripaludis. United States. https://doi.org/10.1128/mbio.00062-13
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Costa, Kyle C., Lie, Thomas J., Jacobs, Michael A., and Leigh, John A. Tue . "H2-Independent Growth of the Hydrogenotrophic Methanogen Methanococcus maripaludis". United States. https://doi.org/10.1128/mbio.00062-13. https://www.osti.gov/servlets/purl/1626081.
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@article{osti_1626081,
title = {H2-Independent Growth of the Hydrogenotrophic Methanogen Methanococcus maripaludis},
author = {Costa, Kyle C. and Lie, Thomas J. and Jacobs, Michael A. and Leigh, John A.},
abstractNote = {Hydrogenotrophic methanogenic Archaea require reduced ferredoxin as an anaplerotic source of electrons for methanogenesis. H2 oxidation by the hydrogenase Eha provides these electrons, consistent with an H2 requirement for growth. Here we report the identification of alternative pathways of ferredoxin reduction in Methanococcus maripaludis that operate independently of Eha to stimulate methanogenesis. A suppressor mutation that increased expression of the glycolytic enzyme glyceraldehyde-3-phosphate:ferredoxin oxidoreductase resulted in a strain capable of H2-independent ferredoxin reduction and growth with formate as the sole electron donor. In this background, it was possible to eliminate all seven hydrogenases of M. maripaludis. Alternatively, carbon monoxide oxidation by carbon monoxide dehydrogenase could also generate reduced ferredoxin that feeds into methanogenesis. In either case, the reduced ferredoxin generated was inefficient at stimulating methanogenesis, resulting in a slow growth phenotype. As methanogenesis is limited by the availability of reduced ferredoxin under these conditions, other electron donors, such as reduced coenzyme F420, should be abundant. Indeed, when F420-reducing hydrogenase was reintroduced into the hydrogenase-free mutant, the equilibrium of H2 production via an F420-dependent formate:H2 lyase activity shifted markedly toward H2 compared to the wild type.},
doi = {10.1128/mbio.00062-13},
journal = {mBio (Online)},
number = 2,
volume = 4,
place = {United States},
year = {Tue Feb 26 00:00:00 EST 2013},
month = {Tue Feb 26 00:00:00 EST 2013}
}
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journal, May 2010

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Anaerobic growth of Methanosarcina acetivorans C2A on carbon monoxide: An unusual way of life for a methanogenic archaeon
journal, November 2004

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journal, August 2012

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    Works referencing / citing this record:

    Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis
    journal, May 2014

    • Lohner, Svenja T.; Deutzmann, Jörg S.; Logan, Bruce E.
    • The ISME Journal, Vol. 8, Issue 8
    • DOI: 10.1038/ismej.2014.82

    Enhanced microbial electrosynthesis by using defined co-cultures
    journal, November 2016

    Metabolic processes of Methanococcus maripaludis and potential applications
    journal, June 2016

    Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater
    journal, September 2018

    A systems level predictive model for global gene regulation of methanogenesis in a hydrogenotrophic methanogen
    journal, October 2013

    • Yoon, Sung Ho; Turkarslan, Serdar; Reiss, David J.
    • Genome Research, Vol. 23, Issue 11
    • DOI: 10.1101/gr.153916.112

    Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens
    journal, February 2019

    • Berghuis, Bojk A.; Yu, Feiqiao Brian; Schulz, Frederik
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 11
    • DOI: 10.1073/pnas.1815631116

    Exploring Hydrogenotrophic Methanogenesis: a Genome Scale Metabolic Reconstruction of Methanococcus maripaludis
    journal, October 2016

    • Richards, Matthew A.; Lie, Thomas J.; Zhang, Juan
    • Journal of Bacteriology, Vol. 198, Issue 24
    • DOI: 10.1128/jb.00571-16
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